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View Proteins belonging to: The Divalent Anion:Na⁺ Symporter (DASS) Family

2.A.47 The Divalent Anion:Na⁺ Symporter (DASS) Family

Functionally characterized proteins of the DASS family (also called the SLC13 family) transport (1) organic di- and tricarboxylates of the Krebs Cycle as well as dicarboxylate amino acid, (2) inorganic sulfate and (3) phosphate. These proteins are found in Gram-negative bacteria, cyanobacteria, archaea, plant chloroplasts, yeast and animals. They vary in size from 432 amino acyl residues (M. jannaschii) to 923 residues (Saccharomyces cerevisiae). The three S. cerevisiae proteins are large (881-923 residues); the animal proteins are substantially smaller (539-616 residues), and the bacterial proteins are still smaller (461-612 residues). They exhibit 11-14 putative transmembrane α-helical spanners (TMSs). An 11 TMS model for the animal NaDC-1 and hNaSi-1 carriers has been proposed (Li and Pajor, 2003; Pajor, 1999). Two serine residues in the human sulfate transporter, hNaSi-1 (Q9BZW2), one in TMS 5 and one in TMS 6, are required for sulfate transport (Li and Pajor, 2003). The former carrier and the other NaDC isoforms cotransport 3 Na⁺ with each dicarboxylate. Protonated tricarboxylates are also cotransported with 3 Na⁺. Several organisms possess multiple paralogues of the DASS family (e.g., 4 for E. coli; 2 for H. influenzae, 3 for S. cerevisiae, and at least 4 for C. elegans).

The phylogenetic tree for the DASS family reveals six clusters as follows: (1) all animal homologues; (2) all yeast proteins; (3) a functionally uncharacterized protein from Ralstonia eutrophus; (4) three E. coli proteins plus one from H. influenzae and one from spinach chloroplasts (the SodiT1 oxoglutarate:malate translocator); (5) an E. coli Orf that clusters loosely with a sulfur deprivation regulated protein of Synechocystis, and (6) an M. jannaschii protein that clusters loosely with an H. influenzae Orf.

Distant homologues of DASS family proteins may include members of the Ars (arsenite exporter) (TC #3.A.4) family as well as the NhaB (TC #2.A.34) and NhaC (TC #2.A.35) Na⁺/H⁺ antiporter families. The DASS family is therefore a member of the ion transporter (IT) superfamily (Rabus et al., 1999).

The generalized transport reaction catalyzed by the DASS family proteins is probably:

Anion^2- (out) + nM⁺ [Na⁺ or H⁺] (out) → Anion^2- (in) + nM⁺ (in).

This family belongs to the: IT Superfamily.

View Proteins belonging to: The Divalent Anion:Na⁺ Symporter (DASS) Family

References associated with 2.A.47 family:

Bun-Ya, M., K. Shikata, S. Nakade, C. Yompakdee, S. Harashima, and Y. Oshima. (1996). Two new genes, PHO86 and PHO87, involved in inorganic phosphate uptake in Saccharomyces cerevisiae. Curr. Genet. 29: 344-351. 8598055

Chen, X.-Z., C. Shayakul, U.V. Berger, W. Tian, and M.A. Hediger. (1998). Characterization of a rat Na⁺-dicarboxylate cotransporter. J. Biol. Chem. 273: 29072-20981. 9694847

Estrella, L.A., S. Krishnamurthy, C.R. Timme, and M. Hampsey. (2008). The Rsp5 E3 ligase mediates turnover of low affinity phosphate transporters in Saccharomyces cerevisiae. J. Biol. Chem. 283: 5327-5334. 18165238

Fei, Y.-J., K. Inoue, and V. Ganapathy. (2003). Structural and functional characteristics of two sodium-coupled dicarboxylate transporters (ceNaDC1 and ceNaDC2) from Caenorhabditis elegans and their relevance to life span. J. Biol. Chem. 278: 6136-6144. 12480943

Hall, J.A., and Pajor A.M. (2007). Functional reconstitution of SdcS, a Na+-coupled dicarboxylate carrier protein from Staphylococcus aureus. J. Bacteriol. 189: 880-885. 17114260

Inoue, K., L. Zhuang, D.M. Maddox, S.B. Smith, and V. Ganapathy. (2002). Structure, function, and expression pattern of a novel sodium-coupled citrate transporter (NaCT) cloned from mammalian brain. J. Biol. Chem. 277: 39469-39476. 12177002

Inoue, K., Y.J. Fei, W. Huang, L. Zhuang, Z. Chen, and V. Ganapathy. (2002). Functional identity of Drosophila melanogaster Indy as a cation-independent, electroneutral transporter for tricarboxylic acid-cycle intermediates. Biochem. J. 367: 313-319. 12186628

Joshi, A.D. and A.M. Pajor. (2009). Identification of Conformationally Sensitive Amino Acids in the Na⁺/Dicarboxylate Symporter (SdcS) (dagger). Biochemistry 48: 3017-3024. 19260674

Kekuda, R., H.P. Wang, W. Huang, A.M. Pajor, F.H. Leibach, L.D. Devoe, P.D. Prasad, and V. Ganapathy. (1999). Primary structure and functional characteristics of a mammalian sodium-coupled high affinity dicarboxylate transporter. J. Biol. Chem. 274: 3422-3429. 9920886

Kim, O.B. and G. Unden. (2006). The L-Tartrate/Succinate antiporter TtdT (YgjE) of L-Tartrate fermentation in Escherichia coli. J. Bacteriol. 189(5): 1597-1603. 17172328

Kovermann, P., S. Meyer, S. Hörtensteiner, C. Picco, J. Scholz-Starke, S. Ravera, Y. Lee, and E. Martinoia. (2007). The Arabidopsis vacuolar malate channel is a member of the ALMT family. Plant J. 52: 1169-1180. 18005230

Li, H. and A.M. Pajor. (2003). Serines 260 and 288 are involved in sulfate transport by hNaSi-1. J. Biol. Chem. 278: 37204-37212. 12857732

Markovich, D., J. Forgo, G. Stange, J. Biber, and H. Murer. (1993). Expression cloning of rat renal Na⁺/SO₄^2- cotransport. Proc. Natl. Acad. Sci. USA 90: 8073-8077. 7690140

Morris, M.E. and H. Murer. (2001). Molecular mechanisms in renal and intestinal sulfate (re)absorption. J. Membrane Biol. 181: 1-9. 11331932

Pajor, A.M. (1995). Sequence and functional characterization of a renal sodium/dicarboxylate cotransporter. J. Biol. Chem. 270: 5779-5785. 7890707

Pajor, A.M. (1999). Sodium-coupled transporters for Krebs Cycle intermediates. Annu. Rev. Physiol. 61: 663-682. 10099705

Pajor, A.M. (2000). Molecular properties of sodium/dicarboxylate cotransporters. J. Membrane. Biol. 175: 1-8. 10811962

Pajor, A.M., N. Sun, L. Bai, D. Markovich, and P. Sule. (1997). The substrate recognition domain in the Na⁺/dicarboxylate and Na⁺/sulfate cotransporters is located in the carboxy-terminal portion of the protein. Biochim. Biophys. Acta 1370: 98-106. 9518567

Pos, K.M., P. Dimroth, and M. Bott. (1998). The Escherichia coli citrate carrier CitT: a member of a novel eubacterial transporter family related to the 2-oxoglutarate/malate translocator from spinach chloroplasts. J. Bacteriol. 180: 4160-4165. 9696764

Rabus, R., D.L. Jack, D.J. Kelly, and M.H. Saier, Jr. (1999). TRAP transporters: an ancient family of periplasmic solute receptor-dependent secondary active transporters. Microbiology 145: 3431-3445. 10627041

Saier, M.H., Jr., B.H. Eng, S. Fard, J. Garg, D.A. Haggerty, W.J. Hutchinson, D.L. Jack, E.C. Lai, H.J. Liu, D.P. Nusinew, A.M. Omar, S.S. Pao, I.T. Paulsen, J.A. Quan, M. Sliwinski, T.-T. Tseng, S. Wachi, and G.B. Young. (1999). Phylogenetic characterization of novel transport protein families revealed by genome analyses. Biochim. Biophys. Acta 1422: 1-56. 10082980

Steffgen, J., B.C. Burckhardt, C. Langenberg, L. K�hne, G.A. M�ller, G. Burckhardt, and N.A. Wolff. (1999). Expression cloning and characterization of a novel sodium-dicarboxylate cotransporter from winter flounder kidney. J. Biol. Chem. 274: 20191-20196. 10400635

Strickler, M.A., J.A. Hall, O. Gaiko, and A.M. Pajor. (2009). Functional characterization of a Na⁺-coupled dicarboxylate transporter from Bacillus licheniformis. Biochim. Biophys. Acta. [Epub: Ahead of Print] 19840771

Teramoto, H., T. Shirai, M. Inui, and H. Yukawa. (2008). Identification of a gene encoding a transporter essential for utilization of C4 dicarboxylates in Corynebacterium glutamicum. Appl. Environ. Microbiol. 74: 5290-5296. 18586971

Urbany, C. and H.E. Neuhaus. (2008). Citrate uptake into Pectobacterium atrosepticum is critical for bacterial virulence. Mol. Plant Microbe Interact. 21: 547-554. 18393614

Wada, M., A. Shimada, and T. Fujita. (2006). Functional characterization of Na⁺ -coupled citrate transporter NaC2/NaCT expressed in primary cultures of neurons from mouse cerebral cortex. Brain Res 1081: 92-100. 16516867

Wang, G., S.P. Kennedy, S. Fasiludeen, C. Rensing, and S. DasSarma. (2004). Arsenic resistance in Halobacterium sp. strain NRC-1 examined by using an improved gene knockout system. J. Bacteriol. 186: 3187-3194. 15126481

Weber, A., E. Menzlaff, B. Arbinger, M. Gutensohn, C. Eckerskorn, and U.-I. Fl�ge. (1995). The 2-oxoglutarate/malate translocator of chlorplast envelope membranes: molecular cloning of a transporter containing a 12-helix motif and expression of the functional protein in yeast cells. Biochemistry 34: 2621-2627. 7873543

Yodoya, E., M. Wada, A. Shimada, H. Katsukawa, N. Okada, A. Yamamoto, V. Ganapathy, and T. Fujita. (2006). Functional and molecular identification of sodium-coupled dicarboxylate transporters in rat primary cultured cerebrocortical astrocytes and neurons. J. Neurochem. 97: 162-173. 16524379